Oxygen and the upper limits to animal design and performance.

Mass-specific rates of aerobic metabolism VO2/Mb) scale in inverse proportion to body mass (Mb). Thus, small hummingbirds display the highest VO2/Mb known among vertebrates. Among all animals, higher VO2/Mb values are known only in flying insects. The high body-mass-specific rates of metabolism seen in hummingbirds are made possible by high lung O2 diffusing capacities, cardiac outputs, ratios of capillary surface area to muscle fiber surface area, mitochondrial volume densities, cristae surface densities and concentrations of enzymes involved in energy metabolism. Current evidence from control analyses of O2 transport through the respiratory and cardiovascular systems and of metabolic fluxes through pathways of energy metabolism indicates shared control of maximum flux rates among multiple steps (i.e. the absence of single rate-limiting steps). This supports the suggestion that functional capacities at each step in linear pathways or processes are matched to each other, and provides an explanation for why the up-regulation of functional capacities has occurred at virtually all steps in the evolution of the smallest vertebrate homeotherms. Flying insects make use of a tracheal system for O2 transport and, like hummingbirds, possess a highly up-regulated biochemical machinery for substrate oxidation. Studies of hummingbirds and honeybees reveal closer matches between biochemical flux capacities and maximum physiological flux rates than in animals capable of lower maximum VO2/Mb. It is proposed that the upper limits to functional capacities set the upper limit to VO2/Mb. This upper limit to aerobic metabolic rate may contribute, along with other factors, towards establishing the lower limit to vertebrate homeotherm size.